The impact of prenatal alcohol and/or tobacco exposure on brain structure in a large sample of children from a South African birth cohort
Andrew T. Marshall
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Search for more papers by this authorStefanie C. Bodison
Department of Occupational Therapy, College of Public Health and Health Professions, University of Florida, Gainesville, Florida, USA
Search for more papers by this authorKristina A. Uban
Department of Public Health, University of California, Irvine, California, USA
Search for more papers by this authorShana Adise
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Search for more papers by this authorDeborah Jonker
Department of Paediatrics and Child Health, University of Cape Town, Cape Town, South Africa
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorWeslin Charles
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorKirsten A. Donald
Department of Paediatrics and Child Health, University of Cape Town, Cape Town, South Africa
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorEric Kan
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Search for more papers by this authorJonathan C. Ipser
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorLetitia Butler-Kruger
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorBabette Steigelmann
Maastricht University, Maastricht, The Netherlands
Search for more papers by this authorKatherine L. Narr
Department of Neurology, UCLA Brain Mapping Center, Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California, USA
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, California, USA
Search for more papers by this authorShantanu H. Joshi
Department of Neurology, UCLA Brain Mapping Center, Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California, USA
Department of Bioengineering, University of California, Los Angeles, Los Angeles, California, USA
Search for more papers by this authorLucy T. Brink
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, California, USA
Search for more papers by this authorHein J. Odendaal
Department of Obstetrics and Gynaecology, Stellenbosch University, Cape Town, South Africa
Search for more papers by this authorFreda Scheffler
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorDan J. Stein
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Unit on Risk and Resilience in Mental Disorders, South African Medical Research Council (SAMRC), Cape Town, South Africa
Search for more papers by this authorCorresponding Author
Elizabeth R. Sowell
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Correspondence
Elizabeth R. Sowell, Department of Pediatrics, Children's Hospital Los Angeles, 4650 Sunset Blvd., Mailstop #130, Los Angeles, CA 90027, USA.
Email: [email protected]
Search for more papers by this authorAndrew T. Marshall
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Search for more papers by this authorStefanie C. Bodison
Department of Occupational Therapy, College of Public Health and Health Professions, University of Florida, Gainesville, Florida, USA
Search for more papers by this authorKristina A. Uban
Department of Public Health, University of California, Irvine, California, USA
Search for more papers by this authorShana Adise
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Search for more papers by this authorDeborah Jonker
Department of Paediatrics and Child Health, University of Cape Town, Cape Town, South Africa
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorWeslin Charles
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorKirsten A. Donald
Department of Paediatrics and Child Health, University of Cape Town, Cape Town, South Africa
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorEric Kan
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Search for more papers by this authorJonathan C. Ipser
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorLetitia Butler-Kruger
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorBabette Steigelmann
Maastricht University, Maastricht, The Netherlands
Search for more papers by this authorKatherine L. Narr
Department of Neurology, UCLA Brain Mapping Center, Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California, USA
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, California, USA
Search for more papers by this authorShantanu H. Joshi
Department of Neurology, UCLA Brain Mapping Center, Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California, USA
Department of Bioengineering, University of California, Los Angeles, Los Angeles, California, USA
Search for more papers by this authorLucy T. Brink
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, California, USA
Search for more papers by this authorHein J. Odendaal
Department of Obstetrics and Gynaecology, Stellenbosch University, Cape Town, South Africa
Search for more papers by this authorFreda Scheffler
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Search for more papers by this authorDan J. Stein
Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa
Neuroscience Institute, University of Cape Town, Cape Town, South Africa
Unit on Risk and Resilience in Mental Disorders, South African Medical Research Council (SAMRC), Cape Town, South Africa
Search for more papers by this authorCorresponding Author
Elizabeth R. Sowell
Department of Pediatrics, Keck School of Medicine, Children's Hospital Los Angeles, University of Southern California, Los Angeles, California, USA
Correspondence
Elizabeth R. Sowell, Department of Pediatrics, Children's Hospital Los Angeles, 4650 Sunset Blvd., Mailstop #130, Los Angeles, CA 90027, USA.
Email: [email protected]
Search for more papers by this authorDan J. Stein and Elizabeth R. Sowell co-senior authors.
Abstract
Background
Neuroimaging studies have emphasized the impact of prenatal alcohol exposure (PAE) on brain development, traditionally in heavily exposed participants. However, less is known about how naturally occurring community patterns of PAE (including light to moderate exposure) affect brain development, particularly in consideration of commonly occurring concurrent impacts of prenatal tobacco exposure (PTE).
Methods
Three hundred thirty-two children (ages 8 to 12) living in South Africa's Cape Flats townships underwent structural magnetic resonance imaging. During pregnancy, their mothers reported alcohol and tobacco use, which was used to evaluate PAE and PTE effects on their children's brain structure. Analyses involved the main effects of PAE and PTE (and their interaction) and the effects of PAE and PTE quantity on cortical thickness, surface area, and volume.
Results
After false-discovery rate (FDR) correction, PAE was associated with thinner left parahippocampal cortices, while PTE was associated with smaller cortical surface area in the bilateral pericalcarine, left lateral orbitofrontal, right posterior cingulate, right rostral anterior cingulate, left caudal middle frontal, and right caudal anterior cingulate gyri. There were no PAE × PTE interactions nor any associations of PAE and PTE exposure on volumetrics that survived FDR correction.
Conclusion
PAE was associated with reduction in the structure of the medial temporal lobe, a brain region critical for learning and memory. PTE had stronger and broader associations, including with regions associated with executive function, reward processing, and emotional regulation, potentially reflecting continued postnatal exposure to tobacco (i.e., second-hand smoke exposure). These differential effects are discussed with respect to reduced PAE quantity in our exposed group versus prior studies within this geographical location, the deep poverty in which participants live, and the consequences of apartheid and racially and economically driven payment practices that contributed to heavy drinking in the region. Longer-term follow-up is needed to determine potential environmental and other moderators of the brain findings here and assess the extent to which they endure over time.
Graphical Abstract
We analyzed brain structure of 332 8- to 12-year-old children from the Prenatal Alcohol, SIDS and Stillbirth (PASS) Network who had varying levels of prenatal alcohol (PAE) and/or tobacco exposure (PTE). PAE was associated with thinner parahippocampal cortices; PTE’s impact was more regionally expansive. Such PAE and PTE effects reflect highly complex downstream outcomes, which require consideration in terms of the amount of exposure, the deep poverty in which participants live, and the legacy of the dop system.
CONFLICT OF INTEREST
The authors declare no conflicts of interest.
Supporting Information
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